The role of macrophage subpopulations in autoimmune disease of the central nervous system

Histochemical Journal

Volumn 28, Issue 2, 1996, Pages 83-97

  Bauer, Jan ^a,b   Ruuls, Sigrid R ^a   Huitinga, Ingeborg ^a   Dijkstra, Christine D ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b Neurological Institute   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; AUTOIMMUNITY; CELL SUBPOPULATION; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; ENCEPHALOMYELITIS; ETIOLOGY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW;

ANIMALS; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; INFLAMMATION; MACROPHAGES; MICROGLIA; MULTIPLE SCLEROSIS;

ANIMALIA;

EID: 0029932436     PISSN: 00182214     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02331413     Document Type: Review

References (104)

1. ANDERSSON, P.-B., PERRY, V. H. & GORDON, S. (1992) The acute inflammatory response to lipopolysaccharide in the CNS parenchyma differs from that of other body tissues. Neuroscience 48, 169-86.
2. BAUER, J., BERKENBOSCH, F., VAN DAM, A.-M. & DIJKSTRA, C. D. (1993) Demonstration of interleukin-1β in Lewis rat brain during experimental allergic encephalomyelitis at the light and ultrastructural level. J. Neuroimmunol. 48, 13-22.
3. BAUER, J., SMINIA, T., WOUTERLOOD, F. G. & DIJKSTRA, C. D. (1994) Phagocytic activity of macrophages and microglial cells during acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neurosci. Res. 38, 365-75.
4. BAUER, J., HUITINGA, I., ZHAO, W., LASSMANN, H., HICKEY, W. F. & DIJKSTRA, C. D. (1995) The role of macrophages, perivascular cells and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 15, 437-46.
5. BOYA, J., CALVO, J. & PRADO, A. (1979) The origin of microglial cells. J. Anat. 129, 177-86.
6. BROADWELL, R. D. & SALCMANN, M. (1981) Expanding the definition of the blood brain barrier to protein. Proc. Natl Acad. Sci. USA 78, 7820-4.
7. BROSNAN, C. F., CAMMER, W., NORTON, W. T. & BLOOM, B. R. (1980) Proteinase inhibitors suppress the development of experimental allergic encephalomyelitis. Nature 285, 235-7.
8. BROSNAN, C. F., BORNSTEIN, M. B. & BLOOM, B. R. (1981) The effects of macrophage depletion on clinical and pathologic expression of experimental allergic encephalomyelitis. J. Immunol. 126, 614-20.
9. BRÜCK, W. & FRIEDE, R. L. (1990) Anti-macrophage CR3 antibody blocks myelin phagocytosis by macrophages in vitro. Acta Neuropathol. 80, 415-18.
10. BUTTER, C., HEALEY, D. G., AGHA, N. & TURK, J. L. (1988) An immunoelectron microscopical study of the expression of Class II MHC and a T lymphocyte surface marker during chronic relapsing experimental allergic encephalomyelitis. J. Neuroimmunol. 20, 45-51.
11. CROSS, A. H., MISKO, T. P., LIN, R. F., HICKEY, W. F., TROTTER, J. L. & TILTON, R. G. (1994) Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelittis in SJL mice. J. Clin. Invest, 93, 268-90
12. COLTON, C. A. & GILBERT D. L. (1987) Production of superoxide anion by a CNS macrophage, the microglial cell. FEBS Lett. 223, 284-8.
13. DAMOISEAUX, J. G. M. C., DÖPP, E. A., NEEFJES, J. J., BEELEN, R. H. J. & DIJKSTRA, C. D. (1989) Heterogeneity of macrophages in the rat evidenced by variability in determinants: two new anti-rat macrophage antibodies against a heterodimer of 160 and 95 kD (CD11/CD18) J. Leukocyte Biol. 46, 556-64.
14. DAMOISEAUX, J. G. M. C., DÖPP, E. A., CALAME, W., CHAO, D., MACPHERSON, G. G. & DIJKSTRA, C. D. (1994) Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology 83, 140-7.
15. DE GROOT, C. J. A, HUPPES, W., SMINIA, T., KRAAL, G. & DIJKSTRA, C. D. (1992) Determination of the origin and nature of brain macrophages and microglial cells in mouse central nervous system, using non-radioactive in situ hybridization and immunoperoxidase techniques. Glia 6, 301-9.
16. DIJKSTRA, C. D., DÖPP, E. A., JOLING, P. & KRAAL, G. (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunol. 54, 589-99.
17. DIJKSTRA, C. D., POLMAN, C. H., KREIKE, A., DE GROOT, C. J. A., KOETSIER, J. C. & SMINIA, T. (1990) The expression of Ia antigen in the course of acute and relapsing experimental allergic encephalomyelitis in the Lewis rat. In Trends in Neuroimmunology (edited by M.G., Marrosu, C. Cinchetti and B. Tavalato) pp. 111-15. London: Plenum Press.
18. DIJKSTRA, C. D., DÖPP, E. A., VAN DEN BERG, T. K. & DAMOISEAUX, J. G. (1994) Monoclonal antibodies against rat macrophages. J. Immmunol. Methods 174, 21-3.
19. DINARELLO, C. A. (1984) Interleukin-1. Rev. Infect. Dis. 6, 51-95.
20. FABRY, Z., WALDSCHMIDT, M. M., HENDRICKSON, D., KEINER, J., LOVEHOMAN, L., TAKEI, F. & HART, M. N. (1992) Adhesion molecules on murine brain microvascular endothelial cells: Expression and regulation of ICAM-1 and Lgp 55. J. Neuroimmunol. 36, 1-11.
21. FUJITA, S. & KITAMURA, T. (1975) Origin of brain macrophages and the nature of so-called microglia. Acta Neuropathol. Suppl. VI, 291-6.
22. GEHRMANN, J. & KREUTZBERG, G. W. (1991) Characterization of two new monoclonal antibodies directed against rat microglia. J. Comp. Neurol. 313, 409-30.
23. GIULIAN, D., BAKER, T. J., SHIH, L.-C. N. & LACHMAN, L. B. (1986) Interleukin 1 of the central nervous system is produced by ameboid microglia. J. Exp. Med. 164, 594-604.
24. GOLD, R. SCHMIED, M., ROTHE, G., ZISCHLER, H., BREITSCHOPF, H., WEKERLE, H. & LASSMANN, H. (1993) Detection of DNA fragmentation in apoptosis: application of in situ nick translation to cell culture systems and tissue sections. J. Histochem. Cytochem. 41, 1023-30.
25. GRAEBER, M. B. & STREIT, W. J. (1990) Perivascular microglia defined. TINS 13, 366.
26. GRABBER, M. B., STREIT, W. J. & KREUTZBERG, G. W. (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cell. J. Neurosci. Res. 21, 18-24.
27. GRAEBER, M. B., STREIT, W. J. & KREUTZBERG, G. W. (1989) Identity of ED2-positive perivascular cells in rat brain. J. Neurosci. Res. 22, 103-6.
28. HARTUNG, H-P., JUNG, S., STOLL, G., ZIELASEK, J., SCHMIDT, B., ARCHELOS, J. J. & TOYKA, K. V. (1992) Inflammatory mediators in demyelinating disorders of the CNS and PNS. J. Neuroimmunol. 40, 197-210.
29. HAYES, G. M., WOODROOFE, M. N. & CUZNER, M. L. (1988) Characterization of microglia isolated from adult human and rat brain. J. Neuroimmunol. 19, 177-89.
30. HETIER, E., AYALA, J., DENÄFLE, P., BOUSSEAU, A., ROUGET, P., MALLAT, M. & PROCHIANTZ, A. (1988) Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J. Neurosci. Res. 21, 391-7.
31. HICKEY, W. F. & KIMURA, H. (1987) Elicitation of MHC gene products and scattered T-lymphocytes in the central nervous sytem of rats by graft versus host disease. Proc. Natl Acad. Sci. USA 84, 2082-6.
32. HICKEY, W. F. & KIMURA, H. (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239, 290-2.
33. HICKEY, W. F., HSU, B. L. & KIMURA, H. (1991) T lymphocyte entry into the central nervous sytem in experimental allergic encephalomyelitis. J. Neurosci. Res. 28, 254-60.
34. HUITINGA, I., VAN ROOIJEN, N., DE GROOT, C. J. A., UITDEHAAG, B. M. J. & DIJKSTRA, C. D. (1990) Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 172, 1025-33.
35. HUITINGA, I., DAMOISEAUX, J. G. M. C., DÖPP, E. A. & DIJKSTRA, C. D. (1993) Treatment with anti-CR3 antibodies ED7 and ED8 suppresses experimental allergic encephalomyelitis in Lewis rats. Eur. J. Immunol. 23, 709-15.
36. HUITINGA, I., RUULS, S. R., JUNG, S., VAN ROOIJEN, N., HARTUNG, H-P. & DIJKSTRA, C. D. (1995) Macrophages in T cell line-mediated, demyelinating, and chronic relapsing experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 100, 344-51.
37. IMAMOTO, K. & LEBLOND, C. P. (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J. Comp. Neurol. 180, 139-63.
38. JACOBS, C. A., BAKER, P. E., ROUX, E. R., PICHA, K. S., TOIVOLA, B., WAUGH, S. & KENNEDY, M. K. (1991) Experimental autoimmune encephalomyelitis is exacerbated by IL-1α and suppressed by soluble IL-1 receptor. J. Immunol. 146, 2983-9.
39. KENNEDY, M. K., TORRANCE, D. S., PICHA, K. S. & MOHLER, K. M. (1992) Analysis of cytokine mRNA expression in the central nervous system of mice with experimental autoimmune encephalomyelitis reveals that IL-10 mRNA expression correlates with recovery. J. Immunol. 149, 2495-505.
40. KESSELRING, J. (1993) Klinik. In Multiple Sklerose (edited by J. Kesselring), 2nd Edn. pp. 95-172. Stuttgart: Kohlhammer.
41. KIM, Y. S. & KIM, S. U. (1991) Oligodendroglial cell death induced by oxygen radicals and its protection by catalase. J. Neurosci. 29, 100-6.
42. KONAT, G. W. & WIGGINS, R. C. (1985) Effect of reactive oxygen species on myelin membrane proteins. J. Neurochem. 45, 1113-8.
43. KONNO, H., YAMAMOTO, T., IWASAKI, Y., SAITOH, T., SUZUKI, H. & TERUNUMA, H. (1989) Ia-expressing microglial cells in experimental allergic encephalomyelitis in rats. Acta Neuropathol. 77, 472-9.
44. LANGEVOORT, H. L., COHN, Z. A., HIRSCH, J. G., HUMPHREY, J. H. SPECTOR, W. G. & VAN FURTH., R. (1970) The nomenclature of mononuclear phagocytic cells. A proposal for a new classification. In: Mononuclear Phagocytes (edited by R. Van Furth), pp. 14-23 Oxford: Blackwell.
45. LASSMANN, H. (1983) Comparative Neuropathology of Chronic Experimental Allergic Encephalomyelitis and Multiple Sclerosis. Berlin: Springer Verlag.
46. LASSMANN, H. (1993) Pathologische Anatomie und experimentelle Modelle. In Multiple Sklerose (edited by J. Kesselring), 2nd Edn, pp. 18-45. Stuttgart: Kohlhammer.
47. LASSMANN, H., KITZ, K. & WISNIEWSKI, H. M. (1980) Structural variability of demyelinating lesions in different models of subacute and chronic experimental allergic encephalomyelitis. Acta Neuropath. 51, 191-201.
48. LASSMANN, H., ZIMPRICH, F., VASS, K. & HICKEY, W. F. (1991) Microglial cells are a component of the perivascular glia limitans. J. Neurosci. Res. 28, 236-43.
49. LASSMANN, H., SCHMIED, M., VASS, K. & HICKEY, W. F. (1993) Bone marrow-derived elements and resident microglia in brain inflammation. Glia 7, 19-24.
50. LAWSON, L. J., PERRY, V. H., DRI, P. & GORDON, S. (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39, 151-70.
51. LIN, R. F., LIN, T. S., TILTON, R. G. & CROSS, A. H. (1993) Nitric oxide localized to spinal cords of mice with experimental allergic encephalomyelitis: an electron paramagnetic resonance study. J. Exp. Med. 178, 643-8.
52. LING, E. A. (1979) Electron microscopical study of macrophages appearing in a stab wound of the brains of rats following intravenous injection of carbon particles. Arch. Histol. Jap. 42, 41-50.
53. LING, E.A., PENNEY, D. & LEBLOND, C.P. (1980) Use of carbon labeling to demonstrate the role of blood monocytes as precursors of the 'amoeboid cells' present in the corpus callosum of postnatal rats. J. Comp. Neurol. 193, 631-57.
54. LININGTON, C., BRADL, M., LASSMANN, H., BRUNNER, C. & VASS, K. (1988) Augmentation of demyelination in rat acute experimental allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am. J. Pathol. 130, 443-54.
55. MCCOMBE, P. A., JERSEY, DE, J. & PENDER, M. P. (1994) Inflammatory cells, microglia and MHC class II antigen-positive cells in the spinal cord of Lewis rats with acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 51, 153-67.
56. MACMICKING, J. D., WILLENBORG, D. O., WEIDEMANN, M. K., ROCKETT, K. A. & COWDEN, W. B. (1992) Elevated secretion of reactive nitrogen and oxygen intermediates by inflammatory leukocytes in hyperactive experimental autoimmune encephalomyelitis: Enhancement by the soluble products of encephalitogenic T-cells. J. Exp. Med. 176, 303-7.
57. MATO, M., OOKAWARA, S. & SAITO-TAKI, T. (1986) Serological determinants of fluorescent granular perithelial cells along small capillary blood vessels in the rodent. Acta Neuropathol. 73, 117-23.
58. MATSUMOTO, Y. & FUJIWARA, M. (1987) Absence of donor-type major histocompatibility complex class I antigen-bearing microglia in the rat central nervous sytem. J. Neuroimmunol. 17, 71-82.
59. MATSUMOTO, Y., HARA, N., TANAKA, R. & FUJIWARA, M. (1986) Immunohistochemical analysis of the rats central nervous system during experimental allergic encephalomyelitis, with special reference to Ia-positive cells with dendritic morphology. J. Immunol. 136, 3668-76.
60. MATSUMOTO, Y., OHMORI, K. & FUJIWARA, M. (1992a) Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J. Neuroimmunol. 37, 23-33.
61. MATSUMOTO, Y., OHMORI, K. & FUJIWARA, M. (1992b) Immune regulation by brain cells in the central nervous system: microglia but not astrocytes present myelin basic protein to encephalitiogenic T-cells under in vivo-mimicking conditions. Immunol. 76, 209-16.
62. MERRILL, J. E., IGNARRO, L. J., SHERMAN, M. P., MELINEK, J. & LANE, T. E. (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151, 2132-41.
63. MIZEL, S. B. (1989) The interleukins. FASEB J. 3, 2379-88.
64. MORIOKA, T. & STREIT, W. J. (1991) Expression of immunomolecules on microglial cells following neonatal sciatic nerve axotomy. J. Neuroimmunol. 35, 21-30.
65. MURABE, Y. & SANO, Y. (1983) Morphological studies on neuroglia. VII. Distribution of 'brain macrophages' in brains of neonatal and adult rats, as determined by means of immunohistochemistry. Cell Tiss. Res. 229, 85-95.
66. NATHAN, C. F. (1987) Secretory products of macrophages. J. Clin. Invest. 79, 319-26.
67. OZAWA, K., SUCHANEK, G., BREITSCHOPF, H., BRÜCK, W., BUDKA, H., JELLINGER, K. & LASSMANN, H. (1994) Patterns of oligodendroglia pathology in multiple sclerosis. Brain 117, 1311-22.
68. PATERSON, P. Y. (1960) Transfer of allergic encephalomyelitis in rats by means of lymph node cells. J. Exp. Med. 111, 119-35.
69. PENDER, M. P. (1987) Demyelination and neurological signs in experimental allergic encephalomyelitis. J. Neuroimmunol. 15, 11-24.
70. PERRY, V. H., HUME, D. A. & GORDON, S. (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15, 313-26.
71. POLMAN, C. H., DIJKSTRA, C. D., SMINIA, T. & KOETSIER, J. C. (1986) Immunohistological analysis of macrophages in the central nervous system of Lewis rats with experimental allergic encephalomyelitis. J. Neuroimmunol. 11, 215-22.
72. RAINE, C. S. (1984) Biology of disease, Analysis of autoimmune demyelination: Its impact upon Multiple Sclerosis. Lab. Invest. 50, 608-35.
73. RIGHI, M., MORI, L., DE LIBERO, G., SIRONI, M., BIONDI, A., MANTOVANI, A. & DENIS DONINI, S., RICCIARDI-CASTAGNOLI, P. (1989) Monokine production by microglial cell clones. Eur. J. Immunol. 19, 1443-8.
74. RINNER, W. A., BAUER, J., SCHMIDTS, M., LASSMANN, H. & HICKEY, W. F. (1995) Resident microglia and hematogenous macrophages as phagocytes in adoptively transferred experimental autoimmune encephalomyelitis: An investigation using rat radiation bone marrow chimeras. Glia 14, 257-66.
75. RIO-HORTEGA, DEL, P. (1919) El 'tercer element' de los centros nerviosos. Bol. Soc. Espan. Biol. 9, 69.
76. ROBINSON A. P., WHITE, T. M. & MASON, D. W. (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. J. Immunol. 57, 239-47.
77. ROSEN, H. (1990) Role of CR3 in induced myelomonocytic recruitment. Insight from in vivo monoclonal studies in the mouse. J. Leukocyte Biol. 48, 465-9.
78. RUULS, S. R., BAUER, J., SONTROP, K., HUITINGA, I., 'T HART, B. A. & DIJKSTRA, C. D. (1995) Reactive oxygen species are involved in the pathogenesis of experimental allergic encephalomyelitis. J. Neuroimmunol. 56, 207-17.
79. SCHELPER, R. L. & ADRIAN, E. K. (1986) Monocytes become macrophages: they do not become microglia: A light and electron microscopic autoradiographic study using 125-iodeoxyuridine. J. Neuropathol. Exp. Neurol. 45, 1-19.
80. SCOLDING, N. J. & COMPSTON, A. S. (1991) Oligodendrocyte-macrophage interaction in vitro triggered by specific antibodies. Immunology 72, 127-32.
81. SCHMIED, M., BREITSCHOPF, H., GOLD, R., ZISCHLER, H., ROTHE, G., WEKERLE, H. & LASSMANN, H. (1993) Apoptosis of T-lymphocytes in experimental autoimmune encephalomyelitis. Evidence for programmed cell death as a mechanism to control inflammation in the brain. Am. J. Pathol. 143, 446-52.
82. SEDGWICK, J. D., SCHWENDER, S., GREGERSEN, R., DORRIES, R. & TER MEULEN, V. (1993) Resident macrophages (resident microglia) of the adult Brown Norway rat central nervous system are constitutively Major Histocompatibility Complex class II-positive. J. Exp. Med. 177, 1145-52.
83. SELMAJ, K. W. & RAINE, C. S. (1988) Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23, 339-46.
84. SIMMONS, R. D., BERNARD, C. C. A., SINGER, G. & CARNEGIE, P. R. (1982) Experimental autoimmune encephalomyelitis. An anatomically-based explanation of clinical progression in rodents. J. Neuroimunol. 3, 307-18.
85. SOBEL, R. A., BLANCHETTE, B. W., BHAN, A. K. & COLVIN, R. B. (1984) The immunopathology of experimental allergic encephalomyelitis. II. Endothelial cell Ia increases prior to inflammatory cell infiltration. J. Immunol. 132, 2402-7.
86. STONE, S. H., SNYDER, D. H. & RAINE, C. S. (1983) Adoptive transfer of experimental allergic encephalomyelitis from immature guinea pig donors. J. Neurol. Sci. 60, 401-9.
87. STREIT, W. J. & KREUTZBERG, G. W. (1987) Lectin binding by resting and reactive microglia. J. Neurocytol. 16, 249-60.
88. STREIT, W. J. & KREUTZBERG, G. W. (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J. Comp. Neurol. 268, 248-63.
89. STREIT, W. J., GRAEBER, M. B. & KREUTZBERG, G. W. (1988) Functional plasticity of microglia: a review. Glia 1, 301-7.
90. SUZUMURA, A., MEZITIS, S. G. E., GONATAS, N. K. & SILVERBERG, D. H. (1987) MHC antigen expression on bulk isolated macrophage-microglia from newborn mouse brain: induction of Ia antigen expression by γ-interferon. J. Neuroimmunol. 15, 263-78.
91. TRAUGOTT, U. & RAINE, C. S. (1985) Multiple sclerosis. Evidence for antigen presentation in situ by endothelial cells and astrocytes. J. Neurol. Sci. 69, 365-70.
92. UITDEHAAG, B. M. J., DE GROOT, C. J. A., KREIKE, A., VAN DER MEIDE, P. H., POLMAN, C. H. & DIJKSTRA, C. D. (1993) The significance of in situ Ia antigen expression in the pathogenesis of autoimmune central nervous system disease. J. Autoimmun. 6, 323-35.
93. VAN DAM, A. M., BROUNS, M., LOUISSE, S. & BERKENBOSCH, F. (1992) Appearance of interleukin-1 in macrophages and in ramified microglia in the brain of endotoxin-treated rats: a pathway for the induction of non-specific symptoms of sickness? Brain Res. 588, 291-6.
94. VAN DAM, A.-M., BAUER, J., MAN-A-HING, W. K. H., MARQUETTE, C., TILDERS, F. J. H. & BERKENBOSCH, F. (1994) Appearance of inducible nitric oxide synthase in the rat central nervous sytem after rabies infection and during experimental allergic encephalomyelitis but not after administration of endotoxin. J. Neurosci. Res. 40, 251-60.
95. VAN FURTH, R. (1982) Current view on the mononuclear phagocyte system. Immunobiol. 161, 178-85.
96. VAN ROOIJEN, N. (1989) The liposome-mediated macrophage 'suicide' technique. J. Immunol. Methods 124, 1-5.
97. VASS, K., LASSMANN, H., WEKERLE, H. & WISNIEWSKI, H. M. (1986) The distribution of Ia antigens in the lesions of rat experimental allergic encephalomyelitis. Acta Neuropathol. 70, 149-60.
98. VAUGHN, J. E. & PETERS, A. (1968) A third neuroglial cell type. An electron microscopic study. J. Comp. Neurol. 133, 269-88.
99. VOORTHUIS, J. A. C., UITDEHAAG, B. M. J., DE GROOT, C. J. A., GOEDE, P. H., VAN DER MEIDE, P. H. & DIJKSTRA, C. D. (1990) Suppression of experimental allergic encephalomyelitis by intraventricular administration of interferon-gamma in Lewis rats. Clin. Exp. Immunol. 81, 183-8.
100. WEKERLE, H. (1988) Intercellular interactions in myelin-specific autoimmunity. J. Neuroimmunol. 20, 211-6.
101. WEKERLE, H., LININGTON, C., LASSMANN, H. & MEYERMANN, R. (1986) Cellular immune reactivity within the CNS. TINS 9, 271-7.
102. WOODROOFE, M. N., HAYES, G. M. & CUZNER, M. L. (1989) Fc receptor density, MHC antigen expression and superoxide production are increased in interferon-gamma-treated microglia isolated from adult rat brain. Immunol. 68, 421-6.
103. YEDNOCK, T. A., CANNON, C., FRITZ, L. C., SANCHEZ-MADRID, F., STEINMAN, L. & KARIN, N. (1992) Prevention of experimental autoimmune encephalomyelitis by antibodies against α4β1 integrin. Nature 356, 63-6.
104. ZIELASEK, J., ARCHELOS, J. J., TOYKA, K. V. & HARTUNG, H.-P. (1993) Expression of intercellular adhesion molecule-1 on rat microglial cells. Neurosci. Lett. 153, 136-9.